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Environmental Correlates for Seed Desiccation Sensitivity of New Caledonian Plant Species

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Environmental Correlates for Seed Desiccation Sensitivity of New Caledonian Plant Species Environmental correlates for seed desiccation sensitivity of New Caledonian plant species By Octavie Toublanc-Lambault, Robin Pouteau, Marion Davezies, Manon Marron, Anthony Pain, Bruno Fogliani, Philippe Marmey* Abstract Efficient in situ and ex situ conservation strategies are urgently needed in biodiversity hotspots, where high concentrations of endemic plant species are undergoing exceptional loss of habitat. In particular, determining seed desiccation sensitivity is a key prerequisite to design storage methods useful for ex situ programs. In this study, we explored seed desiccation sensitivity and its link with phenological and morphological traits as well as with the environmental variables for 45 New Caledonian plant species. Desiccation sensitivity was quantified through RH50, i.e. the relative humidity at which 50% of initial viable seeds died. RH50 was found to be positively associated with the initial seed water content, seed mass, precipitation seasonality, precipitation of the warmest quarter, and presence in rainforest habitats. In contrast, the ability of species to endure desiccation increased in drier habitats such as dry forest. We also found that desiccation sensitivity was consistent at the genus level. These new data provide the basis to establish conservation plans for a large array of plant species in New Caledonia. Moreover, this study may help us to better understand the underlying mechanisms of desiccation sensitivity and to predict desiccation sensitivity of other taxa within the New Caledonian flora on the basis of taxonomy, functional traits and environmental features. *Corresponding Author E-mail: [email protected] Pacific Science, vol. 73, no. 2 December 5, 2018 (Early view) Introduction New Caledonia is an archipelago in the South Pacific Ocean recognized as one of the global biodiversity hotspots (Myers et al. 2000, Roberts et al. 2002). This ca. 18,000 km² archipelago hosts 3371 native plant species, 73% of which are endemic (Jaffre et al. 2001, Morat et al. 2012). The flora of New Caledonia also stands out among other floras for its very distinctive nature: the presence of several primitive groups including the emblematic Amborella trichopoda which is sister to all other extant angiosperms (Soltis et al. 2008), the importance of families belonging to the core Eocene flora, and the presence of intense speciation (Morat et al. 2012). This exceptional biological richness results from a complex biogeographical history and a wide variety of environments including an extreme diversity and specificity of edaphic conditions (Jaffre 1993, Morat 1993, Pillon et al. 2010). The geological history of New Caledonia, with its phase of total submersion at the end of the Eocene, its covering by a slice of oceanic lithospheric mantle during emersion and its sudden re-emersion 37 million years ago, led to the presence of ultramafic substrates now covering more than one third of the main island (Paris 1981, Pelletier 2006), with a flora that has adapted to these edaphic conditions (Isnard et al. 2016, Jaffre 1996, Morat et al. 2012, Pillon et al. 2010). The climate of New Caledonia is affected by tropical and temperate influences. The latter are however reduced by the maritime environment and the quasi-permanent presence of the trade wind (Maitrepierre 2012). There are two main seasons in New Caledonia: a hot or cyclonic season, from January to March, and a cool season, from June to September. Transitions between these two seasons are also distinguished, in particular by the presence of a dry season from August to November, which is characterized by low rainfall and low temperature at night but high temperature during the day. 2 The nature and distribution of actual contrasting habitats observed in New Caledonia are thought to be linked to climatic conditions, topography, substrates, and the effects of human activity. Main vegetation units include a dense evergreen rainforest (called rainforest hereafter), a sclerophyllous forest (dry forest), the maquis, savannas, halophytic vegetation, wetland vegetation, and dense secondary shrublands (Morat et al. 1981). New Caledonian species and their association with these vegetation units have been specified (Jaffre et al. 2001, Morat et al. 2012, Munzinger et al. 2016). Natural habitats have experienced profound shrinkage over the last centuries (Jaffre et al. 1998) and remain highly threatened by urban and economic development, such as mining activities (L'Huillier et al. 2010, Pascal et al. 2008), fire (McCoy et al. 1999), invasive species (Pascal et al. 2006), and climate change (Bellard et al. 2014). Desiccation tolerance is the ability of a seed to survive cellular water withdrawal without irreversible damage and to resume its metabolic activities after rehydration (Leprince and Buitink 2010). Historically, seeds were first classified into two categories, orthodox or recalcitrant, for their response to ex situ storage according to their level of tolerance to desiccation (Roberts 1973). Orthodox seeds can tolerate dehydration without damage, while recalcitrant seeds do not survive dehydration. A third seed class was identified as intermediate, and these seeds tolerate a certain level of dehydration (compared to recalcitrant seeds) but loose viability more rapidly at low temperature than orthodox seeds (Ellis et al. 1990). The observed variability in the level of desiccation tolerated by species favored the hypothesis of a continuum of desiccation tolerance among species (Berjak and Pammenter 1994, Dussert et al. 1999, Sun 1999). Multiple abiotic constraints may have influenced seed ecology and, therefore, biodiversity dynamics (Long et al. 2015, Walck et al. 2011). The ability of a seed to survive desiccation plays a major role in species regeneration (Tweddle et al. 2003). Unlike desiccation tolerant (orthodox) 3 seeds that can survive with a very low moisture content, desiccation sensitive seeds need a high moisture content to remain viable (Berjak and Pammenter 2008). Desiccation sensitive seed plants are most commonly found in humid tropical or subtropical forests, which provide a favorable environment for germination and establishment of young seedlings (Dickie and Pritchard 2002, Tweddle et al. 2003), eventhough long distance dispersal may select for seed dessiccation tolerance, even in tropical and subtropical islands (Carlquist 1974). In contrast, desiccation tolerant seed plants are widely represented in drier environments (Delgado and Barbedo 2012, Hong and Ellis 1998). Approximately 92% of the known species of flowering plants bear desiccation tolerant seeds (Long et al. 2015). Of the 8% of known species with desiccation sensitive seeds, some species may however belong to areas with temperate climates (Finch-Savage 1992, Leon-Lobos and Ellis 2002). Desiccation sensitivity was shown to possibly be related to phenology (Daws et al. 2005, Daws et al. 2006, Hong and Ellis 1997, Hong and Ellis 1998) and season specificities (Dussert et al. 2000, Tweddle et al. 2003) and appeared to occur in all the major seed-plant taxonomic groups (Dickie and Pritchard 2002, Wyse and Dickie 2017). There is an urgent need to improve our knowledge of seed ecology in hotspots in order to conserve their outstanding biodiversity. In determine whether seed desiccation sensitivity is correlated with environmental factors, a study was conducted on seeds of species collected in different locations in New Caledonia. Morphological data and physiological results combined with data of bioclimatic variables were analyzed. Such an analysis may be useful in predicting possible adaptation of the species to disturbed environments and in determining suitable strategies for ex situ conservation. 4 MATERIALS AND METHODS Seed collection and measurements The Noumea (NOU) herbarium database (http://herbier-noumea.plantnet-project.org) was used to extract information on species occurrences, habitat distribution, fruiting season, and accessibility. Field missions were conducted to collect seeds or label plants likely to produce fruits in the near future. Harvested seeds were temporarily placed in plastic bags in the field then stored at room temperature (average temperature of 25°C) in darkness up to two days until analysis in the laboratory. For each collected species, we recorded the following information: the type of vegetation in which the species was found, GPS coordinates, the type of fruit and its color at maturity, the number of seeds per fruit, seed length, and the mass of seeds. Length measurements were made on 10 seeds per species then averaged. Mass measurements were made several times per species (with a variable number of seeds depending on the species, ranging from 1 to 100) then averaged to 10 seeds. Scarification or treatment according to local and common usage was applied to some species (i.e. scarification for Alphitonia neocaledonica, rinsing with soap liquid for Pittosporum species) when necessary. Seed desiccation sensitivity assays -1 Water content (WC) was expressed in percentage of fresh weight basis (% = gH20 x gFW x 100). Initial water content (iWC) was WC of seed within 2 days of collection. Seeds were desiccated using the static method by using a range of atmospheres whose relative humidity varied between 9 and 92% at 25°C (Dussert et al. 1999). Nine relative humidity (RH) levels were obtained using saturated salt solutions of KOH, C2H3KO2, MgCl2, K2CO3, NH4NO3, NaCl, (NH4)2SO4, KCl and KNO3 for a RH of 9%, 23%, 34%, 45%, 62%, 75%, 81%, 85%, and 92%, 5 respectively.
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